Abnormal white and gray matter functional connectivity is associated with cognitive dysfunction in presbycusis

Author:

Wang Yao12,Gao Yuting1,Zhao Min3,Hu Xin3,Wang Jing3,Han Yu1,Wang Qinghui45,Fu Xinxing67,Dai Zongrui8,Ren Funxin3,Li Muwei9ORCID,Gao Fei3

Affiliation:

1. School of Life Sciences, Tiangong University , Tianjin 300387 , China

2. Tianjin Key Laboratory of Optoelectronic Detection Technology and System, Tiangong University , Tianjin 300387 , China

3. Department of Radiology, Shandong Provincial Hospital Affiliated to Shandong First Medical University , Jinan 250021 , China

4. Department of Radiology , Shandong Provincial Hospital, , Jinan 250021, Shandong , China

5. Shandong University , Shandong Provincial Hospital, , Jinan 250021, Shandong , China

6. Beijing Institute of Otolaryngology , Otolaryngology-Head and Neck Surgery, Beijing Tongren Hospital, , Beijing 100069 , China

7. Capital Medical University , Otolaryngology-Head and Neck Surgery, Beijing Tongren Hospital, , Beijing 100069 , China

8. Department of Biostatistics, University of Michigan Ann Arbor , Ann Arbor, MI 48109 , United States

9. Vanderbilt University Institute of Imaging Science, Vanderbilt University Medical Center , Nashville, TN 37232 , United States

Abstract

Abstract Presbycusis is characterized by high-frequency hearing loss and is closely associated with cognitive decline. Previous studies have observed functional reorganization of gray matter in presbycusis, but the information transmission between gray matter and white matter remains ill-defined. Using resting-state functional magnetic resonance imaging, we investigated differences in functional connectivity (GM-GM, WM-WM, and GM-WM) between 60 patients with presbycusis and 57 healthy controls. Subsequently, we examined the correlation between these connectivity differences with high-frequency hearing loss as well as cognitive impairment. Our results revealed significant alterations in functional connectivity involving the body of the corpus callosum, posterior limbs of the internal capsule, retrolenticular region of the internal capsule, and the gray matter regions in presbycusis. Notably, disrupted functional connectivity was observed between the body of the corpus callosum and ventral anterior cingulate cortex in presbycusis, which was associated with impaired attention. Additionally, enhanced functional connectivity was found in presbycusis between the internal capsule and the ventral auditory processing stream, which was related to impaired cognition in multiple domains. These two patterns of altered functional connectivity between gray matter and white matter may involve both bottom-up and top-down regulation of cognitive function. These findings provide novel insights into understanding cognitive compensation and resource redistribution mechanisms in presbycusis.

Funder

National Natural Science Foundation of China

Taishan Scholars Project of Shandong Province

Tianjin Natural Science Foundation

Shandong Provincial Natural Science Foundation of China

Jinan Science and Technology Development Program of China

Academic Promotion Programme of Shandong First Medical University

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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